Taxonomic review, palaeoecological, and palaeobiogeographical significances of Campanian Tethyan oysters from the North Eastern Desert, Egypt

The Late Cretaceous was a time of high eustatic sea level that enabled extensive epicontinental seaways and carbonate platforms across the Tethyan Realm, providing favorable habitats for oyster communities to flourish. This study focuses on the Campanian Tethyan oysters from the North Eastern Desert of Egypt regarding taxonomy, palaeoecology, and palaeobiogeography. Three oyster species, Nicaisolopha nicaisei (Coquand, 1862), Pycnodonte (Phygraea) vesicularis (Lamarck, 1806), and Ambigostrea bretoni (Thomas and Peron, 1891), were identified from the Campanian succession in two studied sections. The sampled specimens of the genus Nicaisolopha have undergone a systematic palaeontological revision. As a result, N. tissoti (Thomas and Peron, 1891) is considered herein a junior synonym of N. nicaisei (Coquand, 1862). Palaeobiogeographically, the likely primary migration pattern of the studied oysters suggests an east–west trend along the Southern Tethys margin. All identified oysters in this study exhibit a Tethyan affinity and are primarily abundant in two main provinces: the Southern Tethys and the Western Tethys. The macrofaunal contents are categorized into two fossil associations: the Nicaisolopha nicaisei association of the middle-late Campanian age and the Pycnodonte vesicularis association of the late Campanian age. These macrofaunal associations indicate a deepening trend during the middle-late Campanian age, suggesting a transition from shallow inner neritic to middle neritic environments. Additionally, it is observed that Pycnodonteinae tend to grow larger under eutrophic conditions, low-energy environments, and nutrient-rich waters with high carbonate contents.


Materials and methods
The oyster specimens analyzed in this study were collected from two stratigraphic sections located in the North Eastern Desert of Egypt: the Wadi Tarfa and Wadi Umm Omeiyied (Fig. 1).Surface picking was employed for fossil collection from the outcrop, and the specimens were subsequently subjected to washing and preparation in the laboratory for taxonomic identification.In total, 236 oyster specimens were collected.The collected oyster specimens were identified based on their external shell morphology and hinge structures following the systematic palaeontological descriptions by Stenzel 20 , Malchus 4 , Bieler et al. 21and Carter et al. 22 .Several well-preserved specimens from each species were measured for height (H), length (L), and thickness (T) using a Vernier Caliper in millimeters.These measurements facilitated the calculation of critical ratios (H/L, T/L, T/H) that serve as valuable diagnostic indicators for identifying oyster species.Representative macrofossil specimens were photographed and illustrated in Figs. 4 and 6.To better discern intricate shell morphologies, the imaged specimens underwent a coating procedure using ammonium chloride (NH 4 Cl), adhering to the methodology outlined by Feldmann 23 .All studied specimens were deposited in the Geological Museum of Al-Azhar University under the code AZGMCO followed by a running number.

Systematic palaeontology
The studied Campanian successions in the North Eastern Desert are characterized by paucispecific macroinvertebrate communities containing only three oyster species.The classification and descriptive terminology of the studied oyster are primarily based on Stenzel 20 , with some modifications to incorporate more recent systematic revisions proposed by Malchus 4 , Bieler et al. 21, and Carter et al. 22 , who suggested significant changes in the taxonomic categories above the genus level.

Figure 1.
Geological map of the North Eastern Desert with the location of the studied sections (reprinted after Bazeen et al. 10 with permission from Elsevier).This geological map was modified from the geological map of Egypt, Beni Suef sheet-NH36SW (after Klitszch et al. 18 ).
Vol:.(1234567890) Description: Medium-sized, oval or subtriangular, inflated and thick-shelled; subequivalves with a slightly more convex left valve than the right one; attachment area highly variable from very small to large, sometimes limited to the apex of the ribs; initially with numerous rounded radial folds; adductor scars placed on the posterio-ventral margin or subcentrally and variable from kidney-shaped to weakly crescent-shaped; umbo small and approximately orthogyrate; ligament area long or inclined; left valve resilifer long and shallow with well-developed bourrelets, right valve resilifer flat; no chomata; right and left valves are ornamented with a few rounded-crested, not dichotomous, widen ventrally, wavy radial folds crossed by irregular, closely spaced, undulatory, slightly raised commarginal ribs, and separated by equal, rounded interspaces, ending at commissural folds; the radial folds of the left valve are more pronounced and robust when compared to those of the right valve.Remarks: Nicaisolopha nicaisei exhibits significant variations in the number and size of its radial folds, the spacing of its large concentric lamellae, and the degree of convexity of its left valve.These variations have been observed by several authors, including Malchus 4 , who highlighted that distinguishing smaller specimens of N. nicaisei with irregular ribbing from N. lyonsi can be challenging.Additionally, some specimens exhibit sculptured characteristics similar to N. tissoti.Aqrabawi 33 pointed out that young specimens of N. nicaisei may exhibit similarities to N. tissoti.
The collected specimens are characterized by a high degree of morphological variation, which can be categorized into two main stages: the early stage and the late stage, with intermediary forms linking the two.The late stage is characterized by moderate to large size, featuring a strongly convex left valve ornamented with wide  Description: Medium to large-sized, oval to obliquely triangular, slightly higher than long, moderately thickshelled; inequivalves with the left valve larger and strongly convex, while the right valve is small and flat or slightly concave; posterior-dorsal margin concave and geniculate; umbo less incurved, prominent and orthogyrate to slightly opisthogyrate; deep umbonal cavity; well-developed posterior sulcus; attachment area variable in size from small to absent; ligament area obliquely triangular, often longer than high; adductor muscle scar situated near the posterior margin or subcentral, and with an oval to subrounded shape; concentric growth lines, separated by wide interspaces, covered the outer shell.

S.N H L T H/L T/L T/H S.N H L T H/L T/L T/H
Remarks: Strougo 51 and Hewaidy et al. 55 have documented the occurrence of this species in the early Paleocene of Egypt.They concluded that the specimens from the Paleocene deposits exhibit more pronounced commarginal ribs than those found in the Upper Cretaceous.However, these Paleocene-recorded specimens need to be reexamined due to the significant differences between these samples and those of the Upper Cretaceous deposits.

S.N H L T H/L T/L T/H S.N H L T H/L T/L T/H
AZGMCO-43 22   Malchus, 1990 4 from the Cenomanian of the Western Desert resembles Ambigostrea bretoni (Thomas and Peron, 1891) 28 , in terms of its small pointed apex and fine radial ribbing.However, Ambigostrea bretoni distinguishes itself by being larger, relatively flatter, slightly thickershelled, and having distinctive edge grooves.

Palaeoecology and palaeoenvironment
The Campanian stage of the Late Cretaceous period was characterized by a significant transgression, leading to elevated sea levels that inundated continental interiors and formed extensive epicontinental seas.This transgression was a global phenomenon 55,56 , with North Africa, including Egypt, experiencing the emergence of a shallow marine embayment along the Southern Tethys margin.During this period, the region underwent significant transgression, with marine facies deposition reaching as far south as the Taoudeni-Iullemmeden-Chad-Al Kufra-Upper Egypt basins 57 .Therefore, interpreting Egyptian oyster species provides crucial palaeoecological evidence that aids in characterizing the Campanian settings of the Southern Tethys as far-field reflections of climatic and tectono-eustatic drivers.Their presence is linked to high relative sea levels, facilitating the northward spillover of Tethyan waters along the northern African coastline.The studied faunal contents can be classified into two main fossil associations: the Nicaisolopha nicaisei association and the Pycnodonte vesicularis association.

Nicaisolopha nicaisei association
This association is recorded from the lower part of the Campanian Rakhiyat Formation in the Wadi Umm Omeiyied and Wadi Tarfa sections.It forms an oyster bank and is found within two ledges of calcareous siltstone in the Wadi Tarfa section and one ledge of calcareous siltstone in the Wadi Umm Omeiyied section.In the Wadi Tarfa section, the lower oyster bank has an approximate thickness of one meter, while the upper one measures approximately 80 cm.In the Wadi Umm Omeiyied section, the oyster bank has a thickness of about 1.5 m.The www.nature.com/scientificreports/Nicaisolopha nicaisei association comprises two species: Nicaisolopha nicaisei (Coquand, 1862), and Ambigostrea bretoni.Nicaisolopha is a stationary epifaunal oyster characterized by prominent ribbing, and it is adapted for suspension feeding in normal marine salinity conditions.Attachment scars on the left valves exhibit high variability, ranging from very small to large, sometimes limited to the rib apex.The presence of attachment scars on some left valves suggests that the oyster remained attached to hard objects on the sea floor throughout its life 58 .The dominance of epifaunal organisms in this association indicates the predominance of firm, coarse-grained stable substrates 59 .Moreover, the prevalence of suspension feeders suggests an environment primarily influenced by a single source of nutrients, where food detritus is only available in the water.
The Nicaisolopha fossil bank exhibits a notable level of regularity at its base, with approximately 80% of individuals found articulated and around 30% remaining in their original life position.Additionally, the specimens display a high degree of preservation with low levels of fragmentation, suggesting relatively short-distance transportation under a low-energy regime (parautochthonous association) 60 .The prevalence of articulated individuals indicates evidence of a significant mortality event, implying that these organisms were abruptly buried in their habitat by a sudden influx of sediment.This is also supported by the limited occurrence of perforations on the left and right valves, suggesting swift burial in areas with relatively high sedimentation rates.The oyster bank is situated near the base of siliciclastic beds consisting of siltstone, sandy shale, greenish shale, and black shale (Fig. 2).Therefore, based on the palaeontological and sedimentological data, the environmental interpretation suggests that this association thrived under normal marine conditions.It was characterized by low-energy conditions, well-oxygenated water, relatively high sedimentation rates, and a shallow inner neritic environment (Fig. 7) with hard substrates.

Pycnodonte vesicularis association
This monospecific association was established based on a bulk-sample comprising 25 collected specimens of Pycnodonte vesicularis.These specimens were scattered (dispersed packing) in the uppermost part of the Rakhiyat Formation and the lowermost part of the Sudr Formation.The uppermost part of the Rakhiyat Formation primarily consists of grey fissile shale, intermittently interspersed with marly and calcareous shale bands.Nevertheless, the lowermost part of the Sudr Formation is composed of pale brown chalky limestone (Fig. 3c).While most oysters adapt well to various shallow-water environments, the Pycnodonteinae species likely inhabited deeper waters within the continental shelf facies, at depths exceeding 15 meters 31 .Such a preference implies a low sedimentation rate and indicates that these oysters inhabited muddy bottoms, which is indicative of increasingly calm water conditions 3,34,61 .
The studied species is characterized by a strongly convex left valve and a flat to slightly concave right valve.Additionally, most collected specimens lack attachment scars on the left valve.The asymmetrical and inequivalve shape of this species and the absence of attachment scars indicate that this species predominantly existed as a free-lying individual under low-energy conditions and on soft substrates 3,34,60,61 .However, only a few specimens exhibit attachment scars (Fig. 6c3), implying that only a minority of individuals were able to attach themselves to solid substrates on the ocean floor throughout their adult lifespan.
The specimens of Pycnodonte vesicularis collected from the Rakhiyat Formation differ from those collected from the Sudr Formation in terms of their smaller size, thinner shell, and presence of bioerosion.These variations provide valuable insights into the contrasting palaeoecological and palaeoenvironmental conditions prevalent in the uppermost part of the Rakhiyat Formation and the lowermost part of the Sudr Formation.The bioerosion of the specimens collected from the Rakhiyat Formation can be attributed to the ichnogenus Maeandropolydora (Fig. 8).This trace fossil is known to be produced by suspension-feeding spionid polychaetes 54,62 .Moreover, the reduced incidence of perforations penetrating the valve interiors suggests that the organisms likely experienced bioerosion activity throughout their lifespan.This indicated that the relationship between P. (Ph.) vesicularis and polychaetes may be classified as commensalism 61 .Consequently, the uppermost portion of the Rakhiyat Formation was deposited in a deep inner neritic environment (Fig. 7) characterized by normal marine salinity, low rates of sedimentation, and soft substrates.
Based on foraminiferal data 10 , the lowermost portion of the Sudr Formation is interpreted to have been deposited in a middle neritic setting (Fig. 7), characterized by eutrophic conditions and fluctuating oxygenation levels.This portion also displays features of calm water conditions and nutrient-rich waters with high carbonate content.Moreover, the presence of scleobiont traces on the collected Pycnodonte vesicularis from the lower Sudr Formation (Fig. 6a,b) suggests the existence of predators within this community.The environmental conditions in the lower Sudr Formation may have facilitated the development of the comparatively large-sized Pycnodonte vesicularis oysters (Fig. 6a1,a2,b,c1,c2,c3) in comparison to specimens obtained from the underlying Rakhiyat Formation (Fig. 6d).

Palaeobiogeography
In the present study, three Campanian oyster species were recorded from the North Eastern Desert.These include Pycnodonte (Phygraea) vesicularis, Nicaisolopha nicaisei, and Ambigostrea bretoni.It is worth noting that Ambigostrea bretoni may be restricted to the Campanian of the Southern Tethys margin in Egypt 4,6 , Libya 34 , and Tunisia 28 .On the other hand, P. (Phygraea) vesicularis and N. nicaisei are widely distributed, and their palaeobiogeographic range will be further discussed below.

Pycnodonte (Phygraea) vesicularis
This species exhibits a broad temporal and paleogeographic distribution (Fig. 9), spanning from the Coniacian to the Danian 51,53 .This broad distribution emphasizes the species' adaptability to thrive in diverse environments across various geological ages.This eurytopic species first appeared in the southern part of the Tethys Sea in Tunisia.Thus, the Coniacian deposits in the Southern Tethys of Tunisia, as recorded by Schijfsma 63 , provide the oldest so far evidence of the oyster Pycnodonte (Phygraea) vesicularis.Following its first appearance in Tunisia, the species was recorded from Santonian deposits in the Southern Tethys (Egypt) 8,30,64 and the Western Tethys (Belgium) 50 .The presence of this oyster species in geographically distant areas of the Tethys Sea during the Coniacian and Santonian periods suggests that P. vesicularis initially migrated from the Southern Tethys Sea in Tunisia towards the end of the Coniacian.It then expanded its range both eastward to the Santonian of Egypt's northern Tethys coastline and westward to the Western Tethys region, now situated in Belgium.
A second major migratory event for P. vesicularis occurred during the Santonian-Campanian transition, leading to its widespread distribution across the Tethys region during the Campanian (Fig. 9).It has been documented in various Southern Tethys regions, specifically in Tunisia 28 , Morocco 45 , Egypt 6,8,44,64,66 , Libya 52 , Palestine, and Jordan 33 .In addition, the species has been recorded in the Campanian of the Western Tethys, indicating its migration from Belgium to France 38,49 , Spain 67 , and Poland 46 .Additionally, this species has been recorded in the Nigerian post-Santonian deposits 68 .This West African occurrence suggests a probable marine connection between the Tethys regions and West Africa via the Trans-Sahara Epicontinental Sea during the Campanian-Maastrichtian period.
P. vesicularis underwent a significant third migration during the Campanian-Maastrichtian transition, leading to further expansion of its range.Maastrichtian records indicate its presence in the Southern Tethys deposits in Egypt 6,43,69 , Libya (according to Ref. 34 ), and Jordan 33 , along with western Tethyan areas like France 49 , Belgium 70 , and Poland 46,47 .Notably, P. vesicularis extended its distribution to distant locations during the Maastrichtian, including Madagascar 71 , India 53 , and the Southern Atlantic coast in Argentina 61,72 .The Maastrichtian distribution suggests two concurrent secondary migrations that likely occurred during the Campanian-Maastrichtian transition.One trend involved a westward migration from the Trans-Sahara region to the South Atlantic Ocean province through a shallow sea passage.The other migration took place from the Southern Mediterranean eastward, reaching both India and Madagascar.
During the early Paleocene, P. vesicularis is recorded in two instances from the Southern Tethys, specifically Egypt 8,51,73 and Libya 74 .Nonetheless, the absence of the species from Paleocene deposits across its previously extensive geographical range implies that the Southern Tethys population was less affected by the extinction event at the end of the Cretaceous period compared to populations in the North Tethys, Northeastern Tethys, and India.In addition, the Paleocene specimens from the Western Desert of Egypt exhibit notable differences from the Upper Cretaceous specimens, particularly in the presence of stronger commarginal ribs.These variations raise the necessity for re-evaluating this record and reassessing the species' taxonomic status.
Conversely, some authors have proposed that these early Paleocene records might originate from a reworked unit called the Bir Abu Minqar horizon [75][76][77] , which signifies the K/Pg boundary in Egypt's Western Desert.This www.nature.com/scientificreports/suggests that Pycnodonte (Phygraea) vesicularis specimens recovered from these deposits may have been reworked from late Maastrichtian beds, rather than representing an authentic early Paleocene population in situ.The present study agrees with the findings of Strougo 51 and Hewaidy et al. 73 , supporting the statement that Pycnodonte (Phygraea) vesicularis, recorded from the Egyptian Western Desert, is indeed representative of the early Paleocene and not a result of reworking from the Maastrichtian deposits.This conclusion is drawn from the exceptional preservation of the recorded species and the conspicuousness of their specimen's ornamentation.

Nicaisolopha nicaisei
The presence of Nicaisolopha Vialov, 1936 25 in Egypt may be attributed to the potential migration of Nicaisolopha lugubris larvae from the southwestern United States of America to North Africa during the Turonian 5 .The genus has a range extending from the Late Cretaceous to the Quaternary.The earliest documented occurrence of the oyster Nicaisolopha nicaisei is from the Turonian deposits of Algeria in Southern Tethys (Fig. 10), as recorded by Benmansour 78 .The species has been recorded from the Coniacian deposits of the Southern Tethys in Egypt 4,5,9 and Algeria 34 .A wealth of records has been found in the Santonian-Maastrichtian deposits of the Southern Tethys region.Notably, these include the Santonian deposits in Egypt 5,6,8 and Algeria 34 , as well as the Campanian deposits in Egypt [4][5][6]30,32 , Algeria 26,28,34 , and Tunisia 28 . Moreoer, it has been recorded in the uppermost Campanian-Maastrichtian deposits of Libya 34 .Evidence of migration from the Southern Tethys to Western Tethys is supported by its first European occurrence in the Campanian deposits of France 8 .
The persistence of Maastrichtian records in Egypt 4 and Sudan 79 indicates that the area encompassing Egypt and Sudan was submerged under a shallow epicontinental sea during the Maastrichtian age.Additionally, the oyster Nicaisolopha nicaisei has been recorded from the Maastrichtian deposits of the Trans-Saharan Seaway in   35 .This finding raises the possibility of a potential migration route from the Southern Tethys, potentially through the Trans-Saharan Seaway.
In conclusion, during the Late Cretaceous period, the palaeogeography of the European, North African, and southwest Asian branches of the Tethyan Realm was interconnected via seaways, facilitating a broad geographic distribution of the Pycnodonteinae 3,34,81,82 , Flemingostreinae, and Liostreinae.Accordingly, several species within these subfamilies exhibited biogeographical distributions that spanned the basins of South Europe, North Africa, the Middle East, and SouthWest Asia.Moreover, the widespread distribution of the oysters Nicaisolopha nicaisei and P. (Phygraea) vesicularis can be attributed to the dispersal ability of their larvae through marine currents 3 .The changes in the Tethyan currents, shifting from West-East during the Albian-Cenomanian and Coniacian-Santonian periods to East-West during the Campanian-Maastrichtian, may be attributed to the tectonic events that occurred at the Santonian-Campanian transition 34 .Thus, the primary migration pattern of the studied oysters was likely from the Southern Tethys margin towards the East-West direction.The oysters identified in this study exhibit a Tethyan affinity and dominate two main provinces: the Southern Tethys province and the Western Tethys province.

Conclusions
This study focuses on Campanian Tethyan oysters from the Central North Eastern Desert of Egypt, specifically examining their taxonomy, palaeobiogeography, and palaeoecology.Three oyster species were identified from two Campanian successions: N. nicaisei, Pycnodonte (Phygraea) vesicularis, and Ambigostrea bretoni.In this study, N. tissoti (Thomas and Peron, 1891) is considered a junior synonym of Nicaisolopha nicaisei (Coquand, 1862).The palaeobiogeographic analysis suggests the migration of the studied oysters from the Southern Tethys margin in an East-West direction.These oyster species were primarily linked to the Tethyan Realm and are prominent in the Southern Tethys and Western Tethys provinces.The macrofaunal contents examined in the study are categorized into two associations: Nicaisolopha nicaisei association and Pycnodonte vesicularis association.These macrofaunal associations suggest a transition towards deeper environments during the middle-late Campanian, shifting from shallow inner neritic to middle neritic habitats.Furthermore, species within the Pycnodonteinae subfamily tend to grow larger under eutrophic conditions, calm water environments, and nutrient-rich waters with high carbonate contents.

Figure 3 .
Figure 3. Filed photographs of the studied Wadi Tarfa and Wadi Umm Omeiyied sections: (a,b) The lower part of the El-Rakhiyat Formation enriched with Nicaisolopha nicaisei concentrations in the Wadi Tarfa (a) and Wadi Umm Omeiyied (b) sections.(c) The lower part of the Sudr Formation with Pycnodonte (Phygraea) vesicularis.(d) The unconformity boundary between the El-Rakhiyat and El Sudr formations in the Wadi Tarfa section.

Figure 4 .
Figure 4. Nicaisolopha nicaisei (Coquand, 1862) from the Campanian successions of the Wadi Tarfa and Wadi Umm Omeiyied sections, in the North Eastern Desert, Egypt.(a,d) External views of right valves from the El-Rakhiyat Formation in the Wadi Tarfa section.(b,e,h,i) External views of left valves from the El-Rakhiyat Formation in the Wadi Tarfa section.(c) Internal view of the right valve from the El-Rakhiyat Formation in the Wadi Tarfa section.(f,g) External views of left valves from the El-Rakhiyat Formation in the Wadi Umm Omeiyied section.The bar scale is equal to 10 mm.

Figure 7 .
Figure 7.A palaeoenvironmental schematic diagram depicting the temporal and palaeoecological contexts of Nicaisolopha nicaisei association and Pycnodonte vesicularis association.

Figure 8 .
Figure 8. Maeandropolydora isp. on the external left valve of Pycnodonte (Phygraea) vesicularis from the Campanian El-Rakhiyat Formation in the Wadi Tarfa section.
Two hundred specimens were collected from the Campanian Rakhiyat Formation in the Wadi Umm Omeiyied and Wadi Tarfa sections, including 40 complete articulated specimens, 100 left valves, and 60 right valves.